ABSTRACT A 6-year study was conducted to determine the signs, symptoms, and management of repeat concussion in National Football League players.
From 1996 to 2001, concussions were reported by 30 National Football League teams using a standardized reporting form filled out by team physicians with input from athletic trainers. Signs and symptoms were grouped by general symptoms, somatic complaints, cranial nerve effects, cognition problems, memory problems, and unconsciousness. Medical actions taken and management were recorded.
Data were captured for 887 concussions in practices and games involving 650 players. A total of 160 players experienced repeat injury, with 51 having three or more concussions during the study period. The median time between injuries was 374.5 days, with only six concussions occurring within 2 weeks of the initial injury. Repeat concussions were more prevalent in the secondary (16.9%), the kick unit on special teams (16.3%), and wide receivers (12.5%). The ball return carrier on special teams (odds ratio [OR] = 2.08, P = not significant) and quarterbacks (OR = 1.92, P < 0.1) had elevated odds for repeat injury, followed by the tight end (OR = 1.24, P = not significant) and linebackers (OR = 1.22, P = not significant). There were similar signs and symptoms with single and repeat concussion, except for a higher prevalence of somatic complaints in players on their repeat concussions compared with their first concussion (27.5% versus 18.8%, P < 0.05). More than 90% of players were managed by rest, and 57.5% of those with second injuries returned to play within a day. Players with three or more concussions had signs, symptoms, and treatment similar to those with only a single injury.
The most vulnerable players for repeat concussion in professional football are the ball return carrier on special teams and quarterbacks. Single and repeat concussions are managed conservatively with rest, and most players return quickly to play.

[Show abstract][Hide abstract]ABSTRACT:
Background: Current characterizations of chronic traumatic brain injury (CTBI) in boxing, football and other sports are reviewed in the context of the history of research on sub-concussive brain trauma in athletes. Methods: The utility of exposure models for understanding CTBI in boxers is examined and concerns regarding the paucity of findings supportive of an exposure model for CTBI in football players are discussed. Results and conclusions: Recommendations for development of exposure models for sport-specific phenotypic characterizations of CTBI are presented.

[Show abstract][Hide abstract]ABSTRACT:
Primary objective: The aim of this literature review was to systematically describe the sequential metabolic changes that occur following concussive injury, as well as identify and characterize the major concepts associated with the neurochemical cascade. Research design: Narrative literature review. Conclusions: Concussive injury initiates a complex cascade of pathophysiological changes that include hyper-acute ionic flux, indiscriminant excitatory neurotransmitter release, acute hyperglycolysis and sub-acute metabolic depression. Additionally, these metabolic changes can subsequently lead to impaired neurotransmission, alternate fuel usage and modifications in synaptic plasticity and protein expression. The combination of these metabolic alterations has been proposed to cause the transient and prolonged neurological deficits that typically characterize concussion. Consequently, understanding the implications of the neurochemical cascade may lead to treatment and return-to-play guidelines that can minimize the chronic effects of concussive injury.

[Show abstract][Hide abstract]ABSTRACT:
Concussions and subconcussive impacts sustained in American football have been associated with short- and long-term neurologic impairment, but differences in head impact outcomes across playing positions are not well understood. The American Medical Society for Sports Medicine has identified playing position as a key risk factor for concussion in football and one for which additional research is needed. This study examined variation in head impact outcomes across primary football playing positions in a group of 730 NCAA Division I Football Championship Series athletes, using a self-report questionnaire. Although there were no significant differences between position groups in the number of diagnosed concussions during the 2012 football season, there were significant differences between groups in undiagnosed concussions (p=0.008) and "dings" (p<0.001); offensive linemen reported significantly higher numbers than most other positions. Significant differences were found between position groups in the frequencies of several post-impact symptoms including dizziness (p<0.001), headache (p<0.001), and seeing stars (p<0.001) during the 2012 football season, with offensive linemen reporting significantly more symptoms compared to most other groups. There were also positional differences in frequency of returning to play while symptomatic (p<0.001) and frequency of participating in full contact practice (p<0.001). Offensive linemen reported having returned to play while experiencing symptoms more frequently and participating in more full-contact practices than other groups. These findings suggest that offensive linemen, a position group that experiences frequent but low-magnitude head impacts, develop more post-impact symptoms than other playing positions, but do not report these symptoms as a concussion.

Data provided are for informational purposes only. Although carefully collected, accuracy cannot be guaranteed.
The impact factor represents a rough estimation of the journal's impact factor and does not reflect the actual
current impact factor.
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CLINICAL STUDIESCONCUSSION IN PROFESSIONAL FOOTBALL:REPEAT INJURIES—PART 4Elliot J. Pellman, M.D.Mild Traumatic Brain InjuryCommittee, National FootballLeague, New York, New York, andProHEALTH Care Associates, LLP,Lake Success, New YorkDavid C. Viano, Dr. med.,Ph.D.Mild Traumatic Brain InjuryCommittee, National FootballLeague, New York, New York, andProBiomechanics LLC,Bloomfield Hills, MichiganIra R. Casson, M.D.Mild Traumatic Brain InjuryCommittee, National FootballLeague, New York, New York;Department of Neurology, LongIsland Jewish Medical Center,New Hyde Park, New York;Department of Neurology,New York University MedicalCenter, New York, New York; andDepartment of Neurology, AlbertEinstein College of Medicine,Bronx, New YorkAndrew M. Tucker, M.D.Mild Traumatic Brain InjuryCommittee, National FootballLeague, New York, New York, andUniversity of Maryland School ofMedicine, Timonium, MarylandJoseph F. Waeckerle, M.D.Mild Traumatic Brain InjuryCommittee, National Football League,NewYork,NewYork, and Acute Careand Emergency Specialists, MD, PC,Leawood,KansasJohn W. Powell, Ph.D.Mild Traumatic Brain InjuryCommittee, National FootballLeague, New York, New York, andDepartments of Kinesiology andPhysical Medicine andRehabilitation, Michigan StateUniversity, Lansing, MichiganHenry Feuer, M.D.Mild Traumatic Brain InjuryCommittee, National FootballLeague, New York, New York, andIndianapolis Neurosurgical Group,Indianapolis, IndianaReprint requests:David C. Viano, Dr. med., Ph.D.,ProBiomechanics LLC, 265Warrington Road,Bloomfield Hills, MI 48304-2952.Email: dviano@comcast.netReceived, November 11, 2003.Accepted, June 25, 2004.OBJECTIVE: A 6-year study was conducted to determine the signs, symptoms, andmanagement of repeat concussion in National Football League players.METHODS: From 1996 to 2001, concussions were reported by 30 National FootballLeague teams using a standardized reporting form filled out by team physicians withinput from athletic trainers. Signs and symptoms were grouped by general symptoms,somatic complaints, cranial nerve effects, cognition problems, memory problems, andunconsciousness. Medical actions taken and management were recorded.RESULTS: Data were captured for 887 concussions in practices and games involving650 players. A total of 160 players experienced repeat injury, with 51 having three ormore concussions during the study period. The median time between injuries was374.5 days, with only six concussions occurring within 2 weeks of the initial injury.Repeat concussions were more prevalent in the secondary (16.9%), the kick unit onspecial teams (16.3%), and wide receivers (12.5%). The ball return carrier on specialteams (odds ratio [OR] ? 2.08, P ? not significant) and quarterbacks (OR ? 1.92, P? 0.1) had elevated odds for repeat injury, followed by the tight end (OR ? 1.24, P ?not significant) and linebackers (OR ? 1.22, P ? not significant). There were similarsigns and symptoms with single and repeat concussion, except for a higher prevalenceof somatic complaints in players on their repeat concussions compared with their firstconcussion (27.5% versus 18.8%, P ? 0.05). More than 90% of players were managedby rest, and 57.5% of those with second injuries returned to play within a day. Playerswith three or more concussions had signs, symptoms, and treatment similar to thosewith only a single injury.CONCLUSION: The most vulnerable players for repeat concussion in professionalfootball are the ball return carrier on special teams and quarterbacks. Single and repeatconcussions are managed conservatively with rest, and most players return quickly toplay.KEY WORDS: Concussion, Epidemiology, Injury surveillance, Repeat or multiple concussions, Second-impact syndrome, Traumatic brain injuryNeurosurgery 55:860-876, 2004Pbrains of athletes. The areas of concern rangefrom chronic mild or moderate cognitive andmemory impairments to a full-blown chronicencephalopathy syndrome and from an in-creased risk of repeat concussion to prolongedpostconcussion syndrome and the rare but le-thal so-called second-impact syndrome (SIS).Martland (25) first described a syndrome ofchronic brain damage in boxers, presumablyrelated to multiple blows to the head.DOI: 10.1227/01.NEU.0000137657.00146.7Dwww.neurosurgery-online.comhysicians have been concerned for manyyears about the possible deleterious ef-fects of multiple concussions on theIn 1945, Quigley expressed concern aboutrepeat head injuries in other sports by statingthat “three concussions in one season dictateddiscontinuing participation in that sport” (41–43). The influence of this statement persists tothe present time, as indicated by the recom-mendationsof concussionguidelines that players who sustain three con-cussions in one season should be withdrawnfrom play for the remainder of that season (1,6, 11, 37). In the 1970s and 1980s, a number ofarticles raised the specter of the so-called SISand related it to “additive or compoundingmanagement860 | VOLUME 55 | NUMBER 4 | OCTOBER 2004www.neurosurgery-online.com

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effects of minor impact injuries” (41). This rare syndrome hasbeen defined as occurring when “an athlete who has sustainedan initial head injury, most often a concussion, sustains asecond head injury before symptoms associated with the firstare fully cleared” (7).The SIS has been characterized by rapid clinical deteriora-tion resulting from cerebral hyperemia and an increase inintracranial pressure, with a high rate of mortality, after asecond impact to a brain still symptomatic from an initial headinjury. The existence of SIS, as it has been described anddefined, has been questioned (28, 30). However, persistentconcerns about the SIS still influence the authors of currentguidelines, who recommend rigid time intervals that delayreturn to play after many grades of concussion (1, 6, 11, 37).Starting in the 1970s (17) and continuing in recent years,numerous studies have documented the increased cognitiveimpairments seen after repeat concussions compared with thefirst injury (9, 18, 24, 45). These studies have prompted con-cerns about more subtle chronic brain damage caused bymultiple concussions than that seen in the full-blown chronicencephalopathy of boxers.There have been numerous clinical studies defining anddescribing the chronic encephalopathy of boxers (8, 31, 32, 39,40). Clinical studies and relevant animal studies all indicatethat the pattern of chronic brain damage is a result of a largenumber of subconcussive blows to the head over a relativelylong period of time (44). However, this injury has not beenobserved in professional football.In the past 10 years, a number of highly publicized retire-ments of well-known professional athletes after they sustainedmultiple concussions have raised the issue of prolonged orpersistent postconcussion syndrome occurring as a result ofmultiple concussions (15). Over the years, there have also beennumerous reports indicating that players who sustain oneconcussion are at significantly increased risk of sustaining arepeat concussion as well as being more likely to sustain amore serious injury as a result of the repeat concussion (6, 9,16, 18).In dealing with all of these appropriate concerns, treatingphysicians until now have had to rely on personal experience,anecdotal information, case reports, and studies of small num-bers of players with repeat mild traumatic brain injury (MTBI)to aid in their decision-making. The purpose of the presentstudy is to analyze in detail the results of a 6-year prospectivestudy of a relatively large number of repeat concussions in theNational Football League (NFL). It is hoped that this will helpthe medical community to address its numerous concernsregarding the effects of multiple concussions in athletes.In 1994, the NFL formed the Committee on Mild TraumaticBrain Injury in response to safety concerns regarding headinjuries. Background on the committee has been provided byPellman (33). Its mission was to investigate MTBI in the NFLby various scientific methods.The MTBI Committee undertook a series of researchprojects aimed at defining concussion biomechanics in profes-sional football. On the basis of analysis of game video andlaboratory reconstruction of severe impacts using instru-mented test dummies, the biomechanics of concussion hasbeen determined for professional players. This has includeddata on the head acceleration of injury (36) and the locationand direction of impacts (35).The committee also determined a strong need to monitorthe frequency and to have physician evaluation of MTBI in theNFL and at the same time to identify the clinical signs andsymptoms associated with concussion. The initial study fo-cused on 787 concussions during regular-season NFL games(34). It addressed the signs and symptoms of concussion anddetermined the relative risk by player position. The presentstudy involved all 887 concussions reported over a period of 6years from 1996 to 2001 in practice and all games. During thisperiod, 787 (89%) of 887 concussions occurred in regular-season games. This study discusses repeat concussions inprofessional football, including the clinical signs and symp-toms, medical actions taken, and lost days with single andrepeat injury.PATIENTS AND METHODSThe MTBI Committee devised a simple form for team phy-sicians to complete on observed and reported signs and symp-toms on initial and follow-up examinations whenever theyevaluated a player who sustained concussion. At the NFLlevel, there is close cooperation between team physicians andathletic trainers on player medical issues, and they workedtogether to collect cases and data for this study. All playerswere examined by team physicians, and all management de-cisions were made by physicians. During the study period,two teams were added to the NFL. This registry of concus-sions involved MTBI data from 30 teams in the NFL. Themedian number of concussions reported by the teams was 26(range, 6–72) during the study period. Players’ names werenot included on the forms to maintain confidentiality. Theywere identified by a six-digit number.Operational DefinitionsThe definition introduced by the committee in 1996 andused for the study is as follows. A reportable MTBI is a trau-matically induced alteration in brain function, which is man-ifested by alteration of awareness or consciousness, includingbut not limited to being dinged, dazed, stunned, woozy,foggy, amnesic, or, less commonly, rendered unconscious, oreven more rarely, experiencing seizure; or by signs and symp-toms commonly associated with postconcussion syndrome,including persistent headaches, vertigo, light-headedness, lossof balance, unsteadiness, syncope, near-syncope, cognitivedysfunction, memory disturbance, hearing loss, tinnitus,blurred vision, diplopia, visual loss, personality change,drowsiness, lethargy, fatigue, and inability to perform usualdaily activities.The definition is a natural extension of a much earlier onefrom the Ad Hoc Committee to Study Head Injury Nomen-REPEAT CONCUSSION IN PROFESSIONAL FOOTBALLNEUROSURGERYVOLUME 55 | NUMBER 4 | OCTOBER 2004 | 861

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clature of the Congress of Neurological Surgeons (12) and isconsistent with a more recent definition by the AmericanCongress of Rehabilitation Medicine (2).Alteration of AwarenessThere may be occasional difficulty in eliciting a history ofloss of consciousness or a transient alteration in awareness inprofessional football players. Loss of consciousness may bevery short-lived (a few seconds or less) and thus may not bedirectly witnessed by the athletic trainer or medical staff. Inaddition, the player may not want to admit that such an eventoccurred because of a concern that he may lose playing time,although this tendency is waning with a loss of stigma asso-ciated with MTBI. Any player who met the all-inclusive crite-ria as determined by the medical staff and athletic trainers wasincluded as an MTBI case.Signs and SymptomsMTBI is a clinical syndrome that may present with a broadspectrum of signs and symptoms, many of which are nonspe-cific and can be associated with other clinical diagnoses. TheMTBI Committee members who are team physicians in theNFL, as well as MTBI Committee consultants with specialexpertise in the fields of sport neuropsychology and sportneurology, developed a list of the most common signs andsymptoms with concussion. They were grouped into six cate-gories: 1) general symptoms, 2) somatic complaints, 3) cranialnerve findings, 4) cognitive abnormalities, 5) memory prob-lems, and 6) unconsciousness. The checklist was filled out foreach player with a concussion.A purposely large and inclusive list was selected so as tocapture all of the possible clinical signs and symptoms withMTBI in professional football players. The signs and symp-toms that were recorded are consistent with previous medicalliterature on the postconcussion syndrome and the symptomsand signs seen after traumatic brain injury. Most of the itemsare symptoms the player may complain of or the physicianmay elicit by history. Some items are mental status findings(retrograde amnesia, anterograde amnesia, or problems withinformation processing, attention, and immediate recall). Thecommittee did not distribute uniform testing instruments tothe team physicians but rather left the assessment of theseparameters to the discretion of the individual team physicians.The rationale for the various signs and symptoms can befound in a report by Pellman et al. (34).The form also contained questions about physical examina-tion findings, initial management, tests ordered, and disposi-tion regarding return to play as well as information on theequipment worn, impact types, and conditions of the field andplay. A form was generated for each player’s MTBI, includingthe initial evaluation and all subsequent follow-up visits untilthe player was cleared for return to play. Team physicians andtheir consultants used their own evaluation procedures tomanage the injury. The committee did not impose outsidemedical decision-making on the medical staffs of the individ-ual teams. The individual team physicians were to completethe initial and follow-up forms on the basis of their clinicalfindings.Return to PlayThe following definitions apply to the return-to-play aspectof the medical report.? Return immediately: The player returns after an evaluationby the team physician demonstrates that the player is asymp-tomatic. The key here is that the player, because of his relativeposition on the team, may not be called to action for severalminutes. For example, if the player was on the kickoff teamand sustained an MTBI, the physician would perform anevaluation and determine that the player is ready to return,yet, depending on the game, it may be minutes or possibly anhour or so before he actually gets back on the field.? Rest and return: The player is evaluated, and it is deter-mined that there should be some protracted time before adecision is made to return. The key would be that the playerdid eventually return to the same game or practice. An exam-ple might be that the injury occurs in the last 5 minutes of thesecond quarter. Because it is close to halftime, the decision toreturn is not made until the third quarter.? Removed from play: This means that the player was notallowed to return to the game or session in which he wasinjured.? Hospitalized: The player was admitted to the hospital; this isgenerally is characterized as 18 hours or more of hospitaliza-tion. This would mean that going to a local hospital for anx-ray, head computed tomographic scan, or the like and thengoing home would not be classified as “hospitalized.”Days OutThe definition of days out is the time between the date ofinjury and the date that the player was permitted to return tofull and unlimited participation (38). Full and unlimited partic-ipation means that the player must be able to perform all theactivities of the session at the same intensity as his teammates.If a player were in a practice session and was not allowed toparticipate in contact drills, he would not be considered to bereturned to participation, because he was not able to performall of the activities expected of his teammates. In essence, thistells us that on the date of return, the player was expected toparticipate fully in all of the activities that were planned forthe team practice or game.Efforts to Improve ComplianceThe Commissioner of the NFL encouraged all team physi-cians to complete and return forms whenever they examineda player with a head injury. The project was designed torecord information about the injury. The forms were designedfor ease of completion, and the data were limited to thosepoints that would provide the most relevant information onMTBI to improve compliance. The data forms were sent to theNFL epidemiologist and entered into a database with aPELLMAN ET AL.862 | VOLUME 55 | NUMBER 4 | OCTOBER 2004www.neurosurgery-online.com

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blinded coding to maintain anonymity of the players. Whenan initial evaluation form was submitted but the follow-upvisit form was not, committee members contacted team ath-letic trainers and doctors directly to remind them to submitthe follow-up forms. During biannual meetings, the commit-tee monitored the data and discussed findings.Quality AssurancesThe MTBI evaluation forms were logged in by the commit-tee’s epidemiologist and scanned into a database using acommercial software program (Teleforms, Cardiff, CA). Dur-ing the data logging, the individual forms were manuallyreviewed. Each form was then scanned into a temporary da-tabase and verified before being entered into the final data-base. Any fields that were incomplete or inconsistent triggereda follow-up contact with the team athletic trainer or physicianto verify the data. The final database includes informationfrom the initial and follow-up evaluation forms submitted byteam physicians.StatisticsDescriptive statistics were used to characterize those play-ers who had a single concussion and those who had repeatedconcussions during the 6-year study. ?2analyses were used tocompare the presence of individual signs and symptoms,medical action, and management of those with repeat concus-sions with those with a single concussion. t tests were used tocompare the mean number of signs and symptoms for thosewith single and repeated concussions.Odds ratios (ORs) with 95% confidence intervals (CIs) wereused to summarize the magnitude of associations. Paired ttests and the McNemar test were used to compare those sameitems for players on their first and second concussions withinthe 6-year study. Because the number of signs and symptomsmay accumulate in closely spaced injuries, the correlationbetween the change in number of signs and symptoms andtime interval was calculated. A separate analysis was con-ducted on the 51 players with three or more concussions. Thisanalysis included a review of their signs and symptoms foreach injury and days out. Differences between injuries for thesame player were evaluated with the McNemar test. Theresults for the 15 players with four or more concussion (46concussions) were summarized separately.RESULTSRepeat ConcussionTable 1 shows the prevalence of single and repeat concus-sions during the 1996 to 2001 NFL seasons. There were 887reported MTBI cases in practice and preseason, regular-season, and postseason games. This involved 650 players, 160(24.6%) of whom had repeat concussions. Fifty-one concussedplayers (7.9%) experienced three or more injuries, and oneplayer had seven concussions during the study period.The median duration between the first and second concus-sions was 374.5 days (range, 0–1693 d). Of those occurringwithin a 90-day window (n ? 38), the median was 31.5 days.Of these 38 players, 36 received their injuries during regulargames in the same season. Only six concussions occurredwithin 2 weeks of the initial injury.Table 2 shows the prevalence of concussion by player position.It includes the frequency of single and the first of repeat concus-sions over six seasons. As a group, the offensive team has aslightly higher frequency of single and repeat concussions. Indi-vidually, the position groups most often associated with the firstof repeat concussions are the defensive secondary (16.9%), kickunit (16.3%), wide receivers (12.5%), and defensive line (10.0%).The defensive secondary includes the safety and cornerbacks,and wide receivers include flankers and split ends.The ORs in Table 2 show that only two position groups havestatistically elevated odds of repeat concussions. Quarterbacks(OR ? 1.92; 95% CI, 0.99–3.74; P ? 0.1) have higher odds ofrepeat concussion, and the offensive line (OR ? 0.54; 95% CI,0.27–1.08; P ? 0.1) has lower odds. Ball carriers on specialteams (OR ? 2.08; 95% CI, 0.73–5.93) have the highest pointestimate of repeat injury, but the numbers are very small. Theother positions at elevated odds include tight ends (OR ? 1.24;95% CI, 0.58–2.64) and linebackers (OR ? 1.22; 95% CI, 0.63–2.38). There was no difference in proportion of injuries thatoccurred in games versus practice across single concussions(85.9%), first of repeat concussions (87.5%), and second ofrepeat concussions (94.4%).Table 3 summarizes the signs and symptoms for single andrepeat concussions during the 1996 to 2001 seasons. The pres-ence of signs and symptoms for the 490 players with a singleconcussion and 160 players with repeat injuries (on their firstinjury) were compared by use of ?2analysis. The prevalence ofsigns and symptoms was similar for players experiencing oneconcussion and the first of repeat concussions, except for ahigher prevalence of diplopia (P ? 0.01) and lower prevalenceTABLE 1. Single and repeat concussions in the NationalFootball League, 1996–2001No. ofconcussionsplayersNo. ofPercentageTotalconcussions1 490 75.6%4902 10916.8% 2183 365.6% 10848 1.2%3254 0.6% 2062 0.3%12710.2%7Total 650 100%887REPEAT CONCUSSION IN PROFESSIONAL FOOTBALLNEUROSURGERYVOLUME 55 | NUMBER 4 | OCTOBER 2004 | 863

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of personality change (P ? 0.01) in those who later incurred arepeat concussion.The prevalence of somatic complaints was higher at thesecond concussion (P ? 0.05) by use of an analysis that com-pares the presence of signs and symptoms on the initial andrepeat concussions with the McNemar test. Loss of conscious-ness for 1 minute or more ranged from six (1.2%) in thesingle-concussion group to three (1.9%) in the initial and four(2.5%) in the second concussion groups (P ? not significant).With a paired t test, there was no statistical difference in themean number of signs and symptoms from the initial to therepeat concussion. Likewise, there was no correlation betweenthe change in number of signs and symptoms and the timeinterval between the initial and repeat concussions.Table 4 summarizes the medical action taken after injury.The most common action with the player who has a singleconcussion is to remove him from play (50.4%), as it is with theinitial (45.6%) and repeat concussion (41.3%). Of the 36 playerswith a second injury during regular games in the same season,50% were removed from play.Table 5 shows the management of concussion. Overall,97.4% of known cases of the players with repeat concussionwere managed with rest. This is slightly higher than 94.3% forthose with a single concussion. These frequencies are essen-tially similar, because only a few players were given variousdrug therapies or medical procedures, which were not furtherdefined in the medical form.Figure 1 shows days out from play after single and repeat con-cussion. Of the concussed players, 91.9% returned to play within aweek. The proportions of players who were not cleared for play for7 days or more were 7.8% (single injury), 5.0% (initial), and 10.0%(repeat concussions). Of these players, 13.0% were out 7 days orlongerwiththreeormoreconcussions.NotshowninFigure1isthat50% of the players with same-season regular-game second injurywere not cleared for play within 6 days.Three or More ConcussionsTable 6 gives the signs and symptoms and days out for the51 players experiencing three or more concussions in theTABLE 2. Incidence of single and first of repeat concussions in six National Football League seasonsaSingle concussionFirst of repeatconcussionsOddsratio95%confidenceintervalThree or moreconcussionsNo.% No.% No.%OffenseWide receiverRunning backQuarterbackOffensive lineTight endSubtotal57422554252038.6%8.6%5.1%11.0%5.1%41.4%20141510106912.5%8.8%9.4%6.3%6.3%43.1%1.081.021.92b0.54b1.241.070.63–1.870.54–1.920.99–3.740.27–1.080.58–2.640.75–1.538650415.4%11.5%9.6%7.7%44.2% 23DefenseSecondaryDefensive lineLinebackerSubtotal80433315616.3%8.8%6.7%31.8%2716135616.9%10.0%8.1%35.0%1.041.151.221.150.64–1.670.63–2.110.63–2.380.79–1.6865511.5%9.6%9.6%30.8% 16Special teamKick unitReturn unitReturn ball carrierPunterKicker, FGAKicker, PATHolderSubtotal92189811113018.8%3.7%1.8%1.6%0.2%0.2%0.2%26.5%262600003416.3%1.3%3.8%0.840.332.080.52–1.350.08–1.440.73–5.93812000015.4%1.9%3.8%21.3% 0.750.49–1.16 11 21.2%Unknown1 0.2%10.6%3.07 0.19–49.351 1.9%Total 490100% 160100%51100%aFGA, field goal attempt; PAT, point after touchdown.bP ? 0.10 from ?2analysis comparing positions having repeat versus single concussion versus all other positions.PELLMAN ET AL.864 | VOLUME 55 | NUMBER 4 | OCTOBER 2004www.neurosurgery-online.com

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TABLE 3. Signs and symptoms of single and repeat concussions in the National Football League (data on repeat concussions for first,second, and third injury)aSigns and symptomsSingle concussion(n ? 490)Repeat concussionsFirst (n ? 160) Second (n ? 160) Third (n ? 51)General symptomsHeadachesNauseaVomitingNeck painBack painSyncopeSeizures65.1%58.0%9.0%2.4%12.9%0.6%1.4%61.3%56.3%11.9%0.6%11.3%65.0%56.3%6.9%0.6%14.0%64.7%58.8%5.9%15.7%1.9%0.6%1.9%Somatic complaintsIrritabilityAnxietyDepressionPersonality changeFatigueSleep disturbanceLoss of libidoLoss of appetite18.0%2.2%3.5%0.2%5.7%b9.0%1.0%18.8%b3.1%5.6%27.5%b5.0%10.6%1.3%6.9%b10.0%17.6%2.0%5.9%1.9%b8.8%2.0%7.8%2.0%0.4%Cranial nerve effectsDizzinessVertigoTinnitusNystagmusHearing lossDiplopiaPhotophobiaBlurred visionPupil responsePupil size50.8%42.9%3.7%2.7%0.8%53.1%39.4%4.4%1.9%1.3%60.0%44.4%3.1%2.5%1.3%56.9%41.2%3.9%5.9%2.0%1.0%c2.9%13.9%0.6%0.2%5.0%c4.4%19.4%1.3%2.5%6.9%18.8%3.9%11.8%Cognition problemsNot oriented to personNot oriented to placeNot oriented to timeImmediate recall26.7%2.9%5.5%7.1%24.3%29.4%1.9%3.8%7.5%26.3%27.5%3.8%6.9%11.9%26.3%19.6%2.0%2.0%17.6%Memory problemsAttention problemsInformation processingAGA delayedRGA delayed37.8%13.5%16.1%9.8%17.1%39.4%12.5%16.3%10.6%18.8%41.9%15.6%21.3%9.4%17.5%23.5%7.8%5.9%11.8%Unconsciousness (?1 min)All loss of consciousnessAll reported as zero63405 2515410551664 15Mean no. of signs and symptomsRange2.70–122.80–113.10–122.20–12aAGA, anterograde amnesia; RGA, retrograde amnesia. Comparisons were made between single concussion and first of repeat concussions using ?2test or Fisher’sexact test. Comparisons were made between first and second concussions of repeat concussions using the McNemar test.bP ? 0.05.cP ? 0.01.REPEAT CONCUSSION IN PROFESSIONAL FOOTBALLNEUROSURGERYVOLUME 55 | NUMBER 4 | OCTOBER 2004 | 865

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6-year study period. The average duration between concus-sions was 1.05 years for the first and second injuries and 1.20years for the second and third injuries in the study period.Overall, there was a slight decline in the number of signs andsymptoms with increasing number of concussions, but a verysimilar pattern is seen for the first through third injuries. Onlyone symptom/sign was significantly different between theinjuries. Players were more likely to be reported as havingblurred vision on their first concussion than on their third (P? 0.05). The median number of days out is 0 days out for eachgroup. A review of medical action was made, and the propor-tions of removed from play, rest and return, and hospitaliza-tion were similar for the first through fourth concussions. Onaverage, 46% were rested and returned, 37% were removedfromhospitalized.play, 13% returned immediately, and4% wereDISCUSSIONIn this article, the clinical picture of repeat MTBIs is de-scribed in professional football players during a 6-year periodfrom 1996 to 2001. This is the first study that prospectivelycollected clinical data from the treating physicians and athletictrainers of such a large number of repeat concussion cases.This report represents a comprehensive, detailed, scientificallybased attempt to provide the physician who treats athleteswith objective data on which to build evidence-based man-agement and treatment plans, although care must be taken inapplying the information to other age groups and levels ofcompetition. Until recently, there had been few prospectivereports that attempted to look at the effects of repeat MTBIs inathletes. With the increased use of standardized sideline as-sessment tests and user-friendly neuropsychological tests atthe high school and collegiate levels, more evidence-basedstudies are now appearing in the sports medicine literature(18, 21, 27). These recent reports complement our study, al-though there are differences in the approaches taken and thefindings. Before the general discussion of this study and itsimplications are approached, limitations for the research aredescribed. This provides a framework within which to con-sider the study of repeat concussions in the NFL.LimitationsAs with all research, there are limitations to this study. Wedid not collect retrospective data on previous concussion his-tory as part of this study. Some of the players may have hadprevious concussions either in the NFL in the years before thestudy began or during their playing careers in high school,college, or other levels of football. It is also possible that someof the players sustained cerebral concussions at earlier times intheir lives in nonfootball athletic or nonathletic endeavors.TABLE 4. Action taken with players experiencing single andrepeat concussions in the National Football LeagueaAction takenSingleconcussion(n ? 490)Repeat concussionFirst(n ? 160)Second(n ? 160)Return immediately16.9%15.6%11.9%Rest and return29.6%34.4%40.6%Removed from play50.4%45.6%41.3%Hospitalized1.4%1.3% 4.4%Unknown 1.6%3.1% 1.9%aComparison of single versus first of repeat concussions was not significantby ?2analysis.TABLE 5. Management of players experiencing single andrepeat concussions in the National Football LeagueaManagementSingleconcussion(n ? 490)Repeat concussionFirst(n ? 160)Second(n ? 160)Rest88.2%92.5% 94.4%Prescription drug therapy 1.4%1.3% 0.6%Proprietary prescription0.6% 0.6% 1.3%Therapeutic modality 1.0%3.1%0.6%Medical procedures1.6%Immobilization 0.6%0.6%Not recorded 6.5% 1.9%3.1%aComparison of single versus first of repeat concussions was not significantby ?2analysis.FIGURE 1. Graph showing percentage of NFL players returning to prac-tice and games after single (only one) and repeat concussions during the6-year study period versus the days lost from full participation in practiceand games (note: the x-axis does not show equally spaced time intervalspast 13 d lost).PELLMAN ET AL.866 | VOLUME 55 | NUMBER 4 | OCTOBER 2004www.neurosurgery-online.com

Previous concussion history may affect our conclusions re-garding repeat concussions, because a certain number of theconcussions that we labeled as initial concussions may in facthave been repeat concussions for some individual players. Inthis article, the “initial” MTBI does not necessarily mean “firstMTBI.” It means that the case represents the “initial” MTBIduring the study period. The same applies to repeat injuriesthat occur during the study period.The authors also realize that some MTBIs were not reportedby the affected player to team medical personnel and thereforewere not included in this database. Such unreported injuriesmost likely were very mild in nature and associated withrapid recovery to escape detection by very involved NFLathletic trainers and physicians. In addition, although 160(24.6%) of 650 repeat concussions reflects the proportion ofrepeat injuries in this sample, the population of NFL playerschanges year to year: new players enter the league, olderplayers leave the league, and we do not know what number ofplayers who constitute the 1996 population are still in theleague in subsequent years.There was difficulty collecting data on loss of consciousness.The initial data collection sheet did not ask for data regardingloss of consciousness. Once this was corrected, we found thatmany of the reports that were submitted did not answer thequestion in the loss-of-consciousness part of the form; there-fore, we do not have definitive loss-of-consciousness data on acertain number of players. What has been reported are thecases with a known time of unconsciousness and those casesthat reported a zero or no loss of consciousness. Interestingly,there was a failure to find any relationship between loss ofconsciousness and neuropsychological function in one study,calling into question the assignment of primary importance toloss of consciousness in grading severity of concussion (22).The difference between the sum of these two numbers and theoverall size of the group is the unknown or indeterminatecases.It is also important to note that in a multisite study such asthis, there are numerous different examiners. In some cases,different examiners from a given medical staff may evaluatethat team’s players. There was no uniform method of evalu-ation of concussion in this study, which will give rise tovariability in assessments among the 30 teams and, on occa-sion, within the same team. It must be emphasized that play-ers were not cleared to return to play until they were asymp-tomatic, with normal medical examinations, although someplayers may return with headaches.As noted previously, many of the players in the databasehad neuropsychological testing at baseline and/or after MTBI.The results of these neuropsychological test batteries are notcurrently in this database and therefore not part of this report.It is possible that including the results of the neuropsycholog-ical testing on the patients may add information on the cog-nitive effects of repeat concussions. Return-to-play data werecollected on players with initial and repeat concussions. Al-though the medical condition of the player certainly is themost important factor in determining return to play by teamphysicians, there are many other factors that go into the deci-sion of when the player should return to play. The importanceof the player to the team; the importance of the upcominggame to the team; and pressure from owners, players and theirfamilies, coaches, agents, and media certainly may influencethe final decision of when the player returns to play. Theauthors believe, however, that the medical factors regardingthe patient’s recovery are and should be the overriding factsthat guide the team physicians’ decision-making on return toplay. Furthermore, our results apply to NFL-level players, andextrapolation to younger athletes has not been demonstrated.It is clear that differences may exist between MTBI in highschool and professional athletes.Repeat ConcussionsThe present study found that 160 (24.6%) of 650 playerswho sustained an MTBI in the NFL went on to sustain one ormore repeat MTBIs during a 6-year period. There were 490players who sustained only one MTBI. The 160 players whohad a repeat MTBI represent only a small percentage (5.0%) ofthe 3228 NFL players in regular-season games during the6-year study. In addition, only 51 of the 160 players had a thirdMTBI, 15 had four MTBIs, 7 were reported with five MTBIs, 3with six MTBIs , and 1 with seven MTBIs. Overall, there were397 repeat injuries of 160 players in practices and all gamesduring a period of 6 years. These results indicate that, despitepublic and media perceptions, repeat MTBI affects only arelatively small number of NFL players.Nearly all of the NFL players had been evaluated beforetheir entrance into the league at the NFL Combine, which is apredraft evaluation of 330 elite college athletes invited by the32 NFL teams. The Combine is held every February in India-napolis, and it is uncommon to see a prospective professionalplayer who had two or more concussions during his previoushigh school and college experience. However, no effort wasmade to capture the MTBI history of players involved in this6-year NFL study.One of the most frequently quoted articles in the olderliterature is by Gerberich et al. (16). They used questionnairesregarding head injuries mailed to coaches and players repre-senting 103 high school football teams. This retrospectivestudy used no athletic trainer or physician reports and in-cluded no detailed reports of signs and symptoms. The au-thors found that players with a history of previous traumaticloss of consciousness were 4 times more likely than thosewithout such a previous history to sustain a second MTBI withloss of consciousness. Delaney et al. (13, 14) published theresults of two separate retrospective self-report questionnairesbased on Canadian professional football players and univer-sity football and soccer players. They found that 69% of theprofessionals and more than 80% of the college athletes whosustained a concussion reported a second concussion as well.They indicated that a history of previous concussion increasedthe risk of sustaining another MTBI (13, 14). An attempt wasmade to determine whether there was an increased risk ofPELLMAN ET AL.868 | VOLUME 55 | NUMBER 4 | OCTOBER 2004www.neurosurgery-online.com

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repeat concussion after an initial MTBI in the NFL, but thataspect was not covered in this study. Numerous statisticalmeans of approaching the problem have been investigated,but exposure data were not available to determine relativerisk. If we had used exposure data, we would have had tolimit the analysis to game injuries during the regular 16-gameseason. This would miss the intervening MTBIs that occur inpractice and complicate the calculation.Powell and Barber-Foss (38) reported data on the occurrenceof multiple MTBIs in high school athletes of both sexes com-peting in football, wresting, basketball, baseball, softball, fieldhockey, volleyball, and soccer. The data were collected pro-spectively by athletic trainers over a 3-year period. There wereno reports of clinical signs and symptoms or return-to-playdata. A total of 92 players with more than one MTBI werefound, 65 of which occurred during football. Guskiewicz et al.(19) surveyed athletic trainers at high school and college pro-grams over three seasons. There was a total number of 17,549players in these programs. They reported that 131 repeatconcussions occurred during the same season as the initialconcussion (881 initial concussions). Not all players were ex-amined by physicians, and there were no detailed reports ofsigns and symptoms. Only 69% of athletic trainers who wereinitially asked to participate ultimately completed the study(19). The very high incidence of repeat concussions in theabove studies is not consistent with the results of other stud-ies, including the present one, which found that 24.6% of NFLplayers (160 of 650 players) who sustained one MTBI latersustained repeat MTBIs during a 6-year period (an averageannual incidence of 4.1%).Some recent studies have used standardized concussiontests and computerized neuropsychological tests. There havebeen five reports of neuropsychological test results in athleteswith multiple cerebral concussions (9, 10, 23, 26, 45). In thesestudies, the authors relied solely on the athletes’ self-reports ofprevious concussion history to determine their inclusion in thestudy. The studies noted above did not report clinical signsand symptoms, nor did they report physician findings. Four ofthe studies found that athletes with a history of self-reportedprevious concussions performed worse on postconcussionneuropsychological testing than did their counterparts whohad not reported a history of previous concussions. One studyfound no difference in the neuropsychological test resultsbetween the two groups (23). The report did not contain moredetailed clinical information other than the results of these fewneuropsychological tests.One recent study analyzed the results of a general healthquestionnaire completed by 2488 retired NFL players (3). Itreported that 24% of former players had sustained three ormore concussions during their careers. The study was retro-spective, relied completely on unverified self-reports, and didnot involve physician evaluations. The results of Bailes’ study(3) are in marked contrast to the findings of the present studythat only 160 (5%) of 3228 NFL players in the league duringthe 6-year study sustained multiple MTBIs. Although thenumber of players entering and leaving the league compli-cates determination of a precise risk, this value gives a generalestimate over a recent 6-year period. The marked variability ofconclusions in the above-mentioned studies points to one ofthe many strengths of this present study, in that the concus-sion history was obtained from medical documentation ofprospective events, not from retrospective self-reports, inwhich answers depend on how the questions are asked, thecontext of the questioning, and the selective memory of theathletes (30).Guskiewicz et al. (18) reported a prospective National Col-legiate Athletic Association concussion study of 2905 footballplayers over three seasons, of whom 184 (6.3%) had a concus-sion and 12 had a repeat concussion in the same season. Thedata were collected from questionnaires filled out by athletictrainers. No reports from treating physicians were included inthe results. They concluded that there may be an increasedrisk of repeat concussive injuries and there may be a slowerrecovery of neurological function after repeat concussions inthose who have a history of previous concussions. The resultsof this present NFL study do not support those conclusions.There was concern that after a concussion, there may be a 7- to10-day window of increased susceptibility to sustaining an-other concussion. Again, the results of this present NFL studydo not support that conclusion. In fact, the present NFL studyfound that the average time interval between MTBIs was 1year and that relatively few repeat events occurred within thefirst 10 days after injury. Also, although approximately one-half of players went back to play during the same game/session and approximately 90% returned within 1 week, re-current injury caused by an increased vulnerability in theimmediate postconcussion period does not seem to be a factorin our population.Second-impact SyndromeNo cases of SIS were detected during the 6-year period ofthis study in the NFL. One hundred sixty players sustained atotal of 397 repeat concussions, ranging from 2 to 7 per indi-vidual. There were no deaths, prolonged comas, or any evi-dence of diffuse cerebral edema in the patients. Furthermore,there have been no case reports of SIS in the history of theNFL, despite a relatively common occurrence of concussionand the likelihood that some players may fail to report symp-toms of MTBI and thus play despite being symptomatic withMTBI. The anecdotal experience of team physicians is that,occasionally, the medical staff does not learn about a player’sconcussion until after a game.There are a number of possible explanations for the absenceof SIS in NFL players. Most obvious is the small sample sizeversus the expected incidence rate. The incidence of SIS inhigh school and college football is 1 to 2 per 1,500,000 players.Thus, one would need 375 to 750 years to expect to see a caseof SIS, assuming 2000 players involved per year. In addition,patients who are reported to have had SIS are usually adoles-cents or young adults (5, 7, 29, 41). 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acceleration differently from that of an adult. Cerebral edemaafter brain injury in the pediatric population has been welldocumented (4). The overwhelming majority of players in theNFL are more than 22 years of age. Because SIS is thought tobe a very rare occurrence, our sample size of 397 repeatconcussions in 160 players may have been too small to detectsuch a rare event. A number of the case reports of SIS docu-ment autopsy findings showing cerebral contusions or smallsubdural hematomas that have been deemed “insignificant”(7, 41). Perhaps the phenomenon of SIS represents a compli-cation of a focal brain injury more so than true concussion.Fortunately, focal brain injury in the NFL seems to be exceed-ingly rare. It is also possible that the results of the presentstudy demonstrate that SIS does not truly exist in this popu-lation of players.Concussion Management and GuidelinesMany of the currently promulgated guidelines for the man-agement of sports-related concussion have established exclu-sion periods for multiple reasons, one of which is the preven-tion of SIS. This is based at least partially on the belief thateveryone with a symptomatic MTBI is at risk for developingSIS (1). The absence of any cases of SIS in the NFL during this6-year study period or in the history of the NFL suggests thatsuch arbitrary return-to-play guidelines may be too conserva-tive for professional football.Another often-expressed concern of the authors of concussionmanagement guidelines is the occurrence of chronic brain dam-age as a result of multiple head injuries (1). The chronic enceph-alopathy of boxers is a well-accepted and documented clinicaland pathological syndrome (8, 31, 39, 40, 44). The clinical featuresinclude a combination of cerebellar, extrapyramidal, andpyramidal dysfunction, along with cognitive and personalitychanges. This is accompanied by a well-defined neuropatholog-ical picture. The full-blown clinical picture is present in approx-imately 17% of retired boxers (39), but partial or more subtleabnormalities are seen in a much higher percentage (8, 40). Thepresent study was admittedly not the best vehicle to search forevidenceofchronicencephalopathyinprofessionalfootballplay-ers, but it is important to note that no signs or symptoms werefound of significant extrapyramidal, cerebellar, or pyramidaldysfunction in NFL players with repeat concussions. This wasnot a surprising result, because chronic traumatic encephalopa-thy has been reported only in boxers and a few steeplechasejockeys. We are not aware of any cases of this syndrome infootball players. Furthermore, numerous studies have shownthat the occurrence of chronic encephalopathy of boxers is re-lated to length of career and number of professional bouts, not tothe number of knockouts (concussions) sustained (8, 31, 39, 40). Itis well accepted that chronic encephalopathy of boxers resultsfrom the accumulation of damage from multiple subconcussiveblows to the head over a prolonged period of time, not thenumber of concussions sustained (8, 31, 39, 40, 44).There was no evidence of chronic encephalopathy in thisgroup of football players who had sustained a relatively smallnumber of multiple concussions, although, with years of prac-tice and play from high school, college, and professional play,the length of participation in full-contact football is usuallymore than 10 years in most professional athletes. The authorsrealize that there have been a small number of NFL playerswho have retired with prolonged or permanent postconcus-sion syndrome. These players did not have evidence of pyra-midal, extrapyramidal, or cerebellar dysfunction. They did nothave clinical dementia. They clearly did not have chronicencephalopathy such as that seen in boxers.Our questions regarding management (Table 5) were broadin nature and did not allow us to carefully determine specificmanagement strategies of the treating physician. It is stillnoteworthy that only approximately 5% of players with a firstconcussion or multiple concussions received therapeutic mo-dalities, drug treatments, or medical procedures. It is possiblethat managing physicians will provide more definite manage-ment in the future because of the ever-expanding knowledgeon this subject and the availability of more sophisticated test-ing modalities.In analyzing these data, an attempt was made to determinewhether there were any features of a player’s initial concus-sion that might indicate an increased risk of his going on tosustain multiple MTBIs. There were no differences in manage-ment, including time interval until return to play, betweenthose who did not have another MTBI and those who did.Regarding clinical signs and symptoms, there were two sta-tistically significant differences between the groups. Diplopiawas reported more often in players who later went on tosustain a repeat MTBI. Personality change was reported lessoften in players who later went on to sustain a repeat MTBI. Itis uncertain how valuable these differences will be to physi-cians who treat athletes with head injuries. Diplopia, for ex-ample, was a very infrequent symptom in both groups and isa well-known but infrequent occurrence after MTBI (20, 34). Inthis setting, it is often related to IVth or VIth cranial nervedysfunction, but it may also be an indicator of transient brain-stem or ocular muscle dysfunction. This could suggest in-creased severity of injury and thus help explain an increasedrisk of repeat MTBI. Diplopia was reported in 1% of the 490players who had sustained only one concussion (5 players)and 5% of the 160 players who subsequently sustained arepeat MTBI (5 players). Of the 10 players who complained ofdiplopia after an initial MTBI, 5 (50%) subsequently sustaineda repeat MTBI.These results raise the remote possibility that players withdiplopia after an MTBI may be at increased risk of sustaininga subsequent MTBI, but the small number of players involvedsuggests caution in accepting this finding. More likely, therewas another factor involved. Nine of the 18 cases with diplo-pia occurred in the 1997 season in players from seven differentteams (1996, 2 cases; 1998, 1 case; 1999, 2 cases; 2000, 3 cases;2001, 1 case). Because the cases are not evenly distributed intime, there may have been some increased sensitization todiplopia on the part of some physicians in 1997. Also, twoplayers accounted for four cases. 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understand why players with personality change were lesslikely to sustain a repeat MTBI. In view of the small number ofplayers involved, this association is probably clinically insig-nificant. In considering these findings, it may be more impor-tant for clinicians to note that none of the other signs andsymptoms evaluated in this study occurred at any signifi-cantly different frequency between the two groups.Neuropsychological EffectsThere have been previous studies using neuropsychologicaltesting that demonstrate subtle cognitive, attention, and mem-ory impairments that are more prominent in players withmultiple concussions than in those with only one concussion(9, 10, 24, 26, 45). Although many of the players in our studydid undergo neuropsychological testing, these results are notcurrently part of this study. However, the purely clinicalexaminations did not find cognitive and memory impairmentswith greater frequency in players who experienced repeatversus single MTBIs (Table 3). In fact, the data show thatcognitive and memory problems were present almost equallyin players with more than three concussions compared withtheir first and second concussions in the study period.There may be a “practice effect” occurring. This is a well-known phenomenon in neuropsychological testing wherebysubjects perform better on subsequent administrations of thesame tests because of learned responses rather than because ofany true improvement in their abilities. However, it has alsobeen reported that athletes with multiple concussions differfrom those with only one concussion specifically by not dem-onstrating the practice effect on follow-up neuropsychologicaltesting (45). Another possible explanation could be that treat-ing physicians did not aggressively test for cognitive andmemory impairments after the third concussion because theythought it would be present as it had been in previous con-cussions. If the examiner does not specifically pursue cogni-tive and memory questioning, these signs will often be over-looked. It may be that if the results of neuropsychologicaltesting were available on all of the players in our study, thenwe would be able to confirm the findings of earlier studies thatplayers with multiple concussions perform worse on this typeof testing than their counterparts.Three or More ConcussionsAnother part of the data analysis evaluated players whosustained three or more concussions. Table 6 shows the signsand symptoms of the earlier and later concussions of these 51players. In this analysis, the player serves as his own controlfor the history of successive concussions. With the fourth orlater concussion, there was a higher incidence of personalitychange and fatigue, but the difference did not reach statisticalsignificance. The average numbers of signs and symptomswere somewhat lower in the group with four or more MTBIs,but again the difference did not reach statistical significance.The incidence of loss of consciousness at the time of MTBI wasnot different with successive concussions. The time intervalsto return to play were not significantly different between thetwo groups, although they were longer with repeat concussion(Fig. 1). What is most striking to the authors is the markedsimilarity of the signs and symptoms of each of the successiveMTBIs for these players, although there was a trend to moredays out based on the average and percentage of players out7 days or longer with three or more concussions.Overall, the signs and symptoms reported in our study werevery similar between players with single and multiple MTBIs(Tables 3 and 6). The total number of symptoms per case wasessentially the same, except for a slight decrease in those withthree or more concussions. There was a slightly increasedfrequency of anxiety in the second MTBI compared with theinitial event. This may reflect the athlete’s appropriate con-cerns regarding the effect of repeat injury on his health andcareer, rather than being an indicator of cerebral damage.Although there is a trend toward repeat injuries having moretime missed, the symptoms and signs of repeat injuries are sosimilar to those of single injuries that the longer return to playfor repeat injuries may be a result of more conservative care bythe medical staff rather than more severe injury.It is possible that more subtle abnormalities in personalityor behavior occurred after multiple MTBIs but that these weretoo vague and nonspecific to be adequately recorded on thestandardized forms. Certainly, experienced athletic trainersand team physicians often report that a post-MTBI athlete“does not seem right,” even though by all accounts (clinicalexamination, history, neuropsychological testing) he has re-turned to normal (R Barnes, personal communication, 2003). Itis also the perception of some team physicians that less bio-mechanical force is needed to cause the fourth to seventhconcussions in a small percentage of these players. This seemsto be supported by the game video, which shows lower colli-sion velocities and less severe helmet impacts. However, athorough analysis of this possible effect has not been made. Itwould be interesting to study the susceptibility to injury aftermany concussions. Obviously, the time between injuries andthe cumulative effects are additional factors to consider.Incidence of Repeat Concussion by Player PositionThe present study found that ball return carriers, quarter-backs, tight ends, and linebackers had a higher incidence ofrepeat MTBIs than their counterparts (Table 2). The higherincidence was statistically significant only for quarterbacks,even though kick return ball carriers on special teams had thehighest OR of repeat MTBI. Both of these positions are oftensubjected to high acceleration from open-field or blindsidehead impacts at high velocity. The positions at increased riskof multiple MTBIs are the same ones that were found to haveincreased risk of sustaining any MTBI in an earlier study inthis series (34). In recent years, the NFL has implemented andreinforced several rule changes aimed at protecting playersfrom head injury. In addition, helmet manufacturers havedeveloped newer protective equipment that is now in use.Future analysis of ongoing MTBI data may determine what, ifREPEAT CONCUSSION IN PROFESSIONAL FOOTBALLNEUROSURGERYVOLUME 55 | NUMBER 4 | OCTOBER 2004 | 871

43. Thorndike A: Serious recurrent injuries of athletes. N Engl J Med 246:554–556, 1952.44. Unterharnscheidt FJ: Injuries due to boxing and other sports, in Vinken PJ,Bruyn GW (eds): Handbook of Clinical Neurology. Amsterdam, North HollandPublishing Co., 1975, vol 23, pp 527–593.45. Warden D, Bleiberg J, Cameron K, Sun W, Sparling M, Cernich A, Peck K,Reeves D, Walter J, Uhorchok J, Eckland J: The effect of concussion historyon cognitive performance following acute concussion. Neurology 60[Suppl1]:A362, 2003 (abstr).AcknowledgmentsThe NFL’s Committee on MTBI is chaired by Dr. Elliot Pellman and includesrepresentatives from the NFL Team Physicians Society, NFL Athletic TrainersSociety, NFL equipment managers, and scientific experts in the area of traumaticbrain injury, biomechanics, basic science research, and epidemiology. The authorsof this article are members of the committee. The efforts of other committeemembers are gratefully acknowledged, including Douglas Robertson, M.D., MarkLovell, Ph.D., A.B.P.N., Ronnie Barnes, A.T.C., and Jay Brunetti. None of thecommittee members have a financial or business relationship posing a conflict ofinterest to the research conducted on concussion in professional football.The MTBI Committee gratefully acknowledges the insights of the Commis-sioner, Paul Tagliabue, for forming the committee and issuing a charge toscientifically investigate concussion and means to reduce injury risks in football.The encouragement and support from the NFL’s Jeff Pash and Peter Hadhazyare also appreciated.We also appreciate the contributions of all the NFL team physicians andathletic trainers who filled out the MTBI report forms and those of the playerswho consented to participate in the study through a blinded identification in theMTBI database. We thank the staff at Med Sports Systems for their efforts inmanaging the data flow among the various aspects of the project. Without theirsupport, the project could not have been completed.After publication of Part 3 of the NFL MTBI series (34), the committee becameaware of two players with the same six-digit identification number. The last sixdigits of a player’s Social Security number were used and were thought to be aunique identifier. This increased the number of players with concussion by oneand slightly affected the statistics. The data reported in this article reflect theaccurate count of players who experienced concussion during the 6-year collec-tion of data.The committee extends its appreciation to Cynthia Arfken, Ph.D., at WayneState University, who was our epidemiological consultant for statistical analysisof the concussion data. Her insights and involvement were instrumental to theinterpretation of the data.Funding for this research was provided by the NFL and NFL Charities. TheCharities is funded by the NFL Player’s Association and League. Their supportand encouragement to conduct research on concussion is greatly appreciated.COMMENTSPMild Traumatic Brain Injury Committee study. In this report,they have studied 160 repeat mild traumatic brain injuries(MTBIs) out of an initial group of 887 concussions. These werereported in practices and games for 650 players during the1996–2001 football seasons. Their findings corroborated pre-vious studies showing that players involved with high-speedand often unsuspected collisions sustained concussions andthat repeat concussions occurred at a higher incidence in thedefensive secondary, special team tacklers, ball return special-ists, quarterbacks, tight ends, and linebackers. The clinicalexpression of repeat concussion was similar to that of playerswith an initial or single MTBI except for a higher incidence ofsomatic complaints. There were no findings indicating a dif-ellman et al. have provided us with another analysis of thedata derived from the National Football League (NFL)ference in the number of signs or symptoms between theinitial and repeat concussions. The vast majority (92%) of theNFL players with MTBI returned to play within 1 week, andthe average duration between concussions was slightly greaterthan 1 year. They found that 160 of 650 of their players (24.6%)sustained one or more repeat concussions during the 6-yearperiod. This study used team physicians to complete an eval-uation form on those players identified as having sustained anMTBI.The limitations of this study include the fact that neuropsy-chological evaluations were not included in the evaluation ofthe patient or in reaching their management strategies orconclusions. It has been well documented that the clinicalexamination or reported neurological symptoms or signs arenot as sensitive as neuropsychological testing in a concussedathlete. The latter has been shown to be sensitive to the pres-ence of significant cognitive and mental processing deficits,even in a reportedly asymptomatic football player with anormal neurological examination. Also, the players’ concus-sion histories were not known. The fact that they report a 5%concussion rate does not indicate a true ongoing incidence,because there is an annual turnover rate in team personnel.The assessment of long-term consequences is likewise limitedin this brief follow-up in players who continue to be activelyused by the NFL. For several reasons, there may be disincen-tives to report mild cognitive disturbance or symptoms, or itmay be too early for a chronic syndrome to have developed. Iwould urge caution in extrapolation of these data to include amanagement scheme with rapid return of players at otherlevels, as was their practice, in which approximately 60%returned to play during the same game after sustaining MTBI.In regard to the lack of second-impact syndrome (SIS) in NFLplayers, this probably reflects the fact that it is primarily aphenomenon of youngercontactoccurrence.athletes anda rareJulian E. BailesMorgantown, West VirginiaPtribution to the medical literature dealing with repeat concus-sions in athletes. Their data clearly show that special teams,ball return athletes, and quarterbacks are the players mostvulnerable to repeat concussion, and single and repeat athleteswith concussion in more than 90% of the cases have a goodrecovery and quick return to play.Several other important observations are made. Under pro-spective physician-reported circumstances, the actual incidenceof concussions in the NFL is surprisingly low: approximately 3%per year. Furthermore, although repeat concussions occurred toapproximately one-quarter of the players who sustained an ini-tial concussion, the interval for this second concussion was ap-proximately 1 year.The authors also emphasize that there were no cases of SISduring the 6-year period of the study. Indeed, there has neverellman et al., working through the NFL Committee onMTBI, with this article have made another significant con-REPEAT CONCUSSION IN PROFESSIONAL FOOTBALLNEUROSURGERYVOLUME 55 | NUMBER 4 | OCTOBER 2004 | 873

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been a case report of SIS in an NFL football player, althoughthis syndrome must be considered in any athlete with a cere-bral concussion. The fact that it is exceedingly rare, indeedunreported, in the NFL also needs to be considered in thejudgment-making process.The apprehension of chronic encephalopathy developing infootball players from multiple concussions is also somewhattempered by the fact that in the present study, there were noathletes with documented extrapyramidal, cerebellar pyramidal,or pyramidal dysfunction in players with repeat concussions.Neuropsychological testing is now considered the most sen-sitive means of assessing cognitive and memory function afterMTBI. This form of testing is now available and is used by allNFL teams in patients with cerebral concussion. This height-ened awareness clearly is preventive in reducing serious se-quelae from returning to play too soon. Using these tests, wehave discussed definite personality changes and cognitiveimpairment in athletes with multiple concussions, but in mostof them, almost all symptoms and signs clear given an ade-quate time with contact participation.Although the authors well document concussions in theNFL, a note of caution must be made in extrapolating thesedata to college and high school athletes. We have found, forexample, that high school athletes with three or more concus-sions are nine times more likely to have a repeat concussionand more significant abnormalities in the on-field presentationcompared with those athletes with no history of previousconcussion. This supports the increased vulnerability of thebrain to repeat concussive blows. In addition, we have foundthat high school athletes take longer to recover, as determinedby neurocognitive testing, than college athletes, which sug-gests that the “younger” brain may be even more vulnerableto concussive brain injuries (1).Finally, the relatively low incidence of concussion in theNFL may indicate a selective bias in that those athletes whomake it to that level are more resistant to concussive injuriesand those who are not have already been “weeded out” be-cause of previous injuries. Overall, the authors have madeanother significant contribution to the medical literature onathletic concussive injuries.Joseph C. MaroonPittsburgh, Pennsylvania1. Field M, Collins MW, Lovell MR, Maroon JC: Does age play a role in recoveryfrom sports-related concussion? A comparison of high school and collegiateathletes. J Pediatrics 12:546–554, 2003.A50% of players return to the same game, including more than25% of those with loss of consciousness) seems to be at oddswith virtually all published guidelines and consensus state-ments on managing concussion.In truth, all those guidelines and consensus statements weregenerated from data on high school and college athletes.t first glance, the NFL experience with single and repeatconcussion (no difference) and management (more thanThose in the NFL are not only the most skilled football playersbut also probably the best physically and genetically equippedto withstand the trauma of football, or they never would havebeen accepted on an NFL team. Thus, these authors may bestudying unique individuals.Other explanations can be found by reading and reflectingcarefully on the Limitations section of this article, which isfound at the beginning of the Discussion section. Because theathletes’ previous concussion histories were not obtained, wereally do not know how many concussions these athletesreceived, and therefore, comparisons between first, second,and third concussions in this study do not necessarily reflectthe athlete’s first, second, or third concussion. It can be arguedthat this makes all comparisons suspect.Another concern is this study, understandably, is a 6-yearwindow during which there was turnover of players; thus,comments about not seeing SIS or traumatic encephalopathycould reflect the limited period of exposure.All of the above being said, I find that this article comes ata most interesting time. In the past several years, multiplearticles have been published that place the incidence of con-cussion, based on direct questioning of the athlete, to be 40 to70% annually, not less than 10% as routinely reported bytrainers (Table C1) (2–4; Woronzoff, personal communication,2001). Thus, the incidence of concussion is clearly much higherthan that seen by the medical team on the sidelines, with mostathletes with minor concussions continuing to play. The factthat the athletes questioned did not seem to have problems, asevidenced by their behavior, suggests that further reflectionon the management of minor concussions might be appropri-ate. This article also supports the concept that concussionseverity should be determined not on the day of injury butrather only after concussion symptoms have cleared (1). I amsure these findings will be deliberated at the second interna-tional concussion conference in Prague in November 2004.Robert C. CantuConcord, Massachusetts1. Cantu RC: Concussion severity should not be determined until all postconcussion symptoms have abated. Lancet 3:437–438, 2004.TABLE C1. Incidence: player survey dataSeries (ref. no.)Level IncidenceLangburt et al., 2001 (4)High school47.2%Delaney et al., 2002 (3) College 70.2%Delaney et al., 2000 (2)Canadian FootballLeague47.8%Woronzoff, 2001(personal communication)College 61.2%PELLMAN ET AL.874 | VOLUME 55 | NUMBER 4 | OCTOBER 2004www.neurosurgery-online.com